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Nutrients 2013, 5, 2268-2275; doi:10.3390/nu5072268 OPEN ACCESS

nutrients ISSN 2072-6643 www.mdpi.com/journal/nutrients Article

Vitamin D Status Is Associated with Disease Activity among Rheumatology Outpatients Zohreh Sabbagh 1, Janet Markland 1 and Hassanali Vatanparast 2,* 1

2

Department of Internal Medicine, College of Medicine, University of Saskatchewan, Saskatoon, SK S7J 5B6, Canada; E-Mails: [email protected] (Z.S.); [email protected] (J.M.) Division of Nutrition and Dietetics, College of Pharmacy and Nutrition, School of Public Health, University of Saskatchewan, Saskatoon SK S7N 5C9, Canada

* Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +1-306-996-6341; Fax: +1-306-966-6377. Received: 27 March 2013; in revised form: 6 June 2013 / Accepted: 6 June 2013 / Published: 26 June 2013

Abstract: The co-existence of high prevalence of vitamin D inadequacy among Canadians and high prevalence of systematic autoimmune rheumatic diseases (SARDs) raise the question on relationship between the two situations. Objective: To determine vitamin D status in known cases of common SARDs and compare to those with non-autoimmune diseases; further, to evaluate the impact of vitamin D on disease activity in rheumatoid arthritis (RA) cases. Methods: In a retrospective case-control study design, we evaluated 116 patients in a community clinic classified in two groups, Control group: patients with non-rheumatic disease (n = 56), and Case group: those with rheumatic diseases (n = 60). We compared plasma vitamin D status (25(OH)D), indicators of disease activity and other potential confounders. Further, we determined factors associated with disease activity in RA cases. Results: The plasma 25(OH)D was significantly lower in Case group (64.8 ± 29.8) compared to Control group (86.8 ± 37.7). High number of SARDs outpatients 56%) had considerably low plasma 25(OH)D concentration. RA cases with low plasma 25(OH)D had over five times higher risk of disease activity (OR = 5.15 95% CI 1.16, 22.9; p = 0.031). Conclusion: Inadequate vitamin D status in SARDs cases, along with considerably strong association with disease activity in RA cases, indicate the need for proper evaluation of vitamin D status in this clinical population. Moreover, appropriate training should be given to the patients to ensure the intake of the recommended amount of vitamin D per day through diet or supplement.

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Keywords: rheumatic disease; rheumatoid arthritis; vitamin D; inflammation; disease activity

1. Introduction Systematic autoimmune rheumatic disorders (SARDs) are a cluster of chronic autoimmune disorders associated with significant mortality and morbidity in developed countries, including Canada [1]. Rheumatoid arthritis (RA) as the most common disease in this group, affects around 0.9% of Canadian population; which will increase to 1.3% over the next 30 years [2]. The chronic progressive nature of the disease disables over 50% of cases within 10 years if not treated properly [2]. Early diagnosis and proper intervention strategies are key factors in managing the SARDs and decreasing the burden of disease. Since the prevalence of SARDs is affected by genetic and environmental factors [3], nutrition intervention might have impact in disease prevention and risk reduction. The co-existence of a high prevalence of vitamin D inadequacy among Canadians, particularly in long winters [4], and the high prevalence of SARDs may raise the question on the relationship between these two. Vitamin D is traditionally known for its role in bone mineral homeostasis [5]. However, recent research reveals the existence of vitamin D receptors (VDR) in a variety of cells including anti-presenting cells (APC) [3,5,6]. This indicates the influence of vitamin D in various physiologic processes; one of them is the immune system. Active metabolite of vitamin D (1,25(OH)2D) inhibits the synthesis of IL-1, IL-6, IL-12 and TNF-α by macrophages [7]. It also decreases MHC-II expression on cell surface and molecules such as CD86, CD80 and CD 40 [3,7]. Finally, it increases apoptosis induced by DC and T lymphocytes. Animal studies report the role of vitamin D in preventing autoimmune encephalomyelitis, systemic lupus erythematosus (SLE), collagen-induced arthritis, and inflammatory bowel disease [7]. Along with these findings, evidence suggests an increase in the emergence of self-reactive T cells where the development of immune system co-exists with low vitamin D status [7]. All this evidence suggests vitamin D deficiency might trigger an autoimmune response and appropriate vitamin D status presents immunosuppressive effect [7]. A systematic review of studies on vitamin D and SARDs reported, comparing to healthy control groups, many case-control studies found lower vitamin D status in SARDs cases including SLE, RA,  ankylosing spondylitis, scleroderma, Type 1 diabetes, Multiple Sclerosis and Crohn’s disease [8]. Further, current evidence from mainly small scale heterogeneous studies indicate possible role of vitamin D in improving disease activity in SARD cases such as RA, Multiple Sclerosis, type 1 diabetes, SLE and Crohn’s disease [8]. The association between vitamin D status and diseases activity in RA was evaluated in a recent meta-analyses of current studies including data from three cohort, six cross-sectional and two case-control studies (n = 215,757) [9]. Song et al. report inverse association between RA disease activity and serum vitamin D levels [9]. Recent advances in the role of vitamin D in various diseases and very limited dietary sources has promoted the intake of vitamin D, particularly in Canada’s high latitude areas with long winters such as Saskatoon [4,10], where vitamin D synthesis through sun is limited for at least seven months of the year. However, whether adult patients diagnosed with common autoimmune diseases in Canada have adequate levels of serum vitamin D is not known. The purpose of this study is to determine serum vitamin D status of known cases of common

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autoimmune diseases and compare to those with non-autoimmune diseases; also to evaluate the impact of vitamin D on disease activity. 2. Materials and Methods In a retrospective case-control study design, we evaluated the charts of over 4000 patients and selected 116 patients with measured plasma 25-hydoxy vitamin D (25(OH)D). Using information on final diagnosis we categorized patients in case and control groups; 60 patients with autoimmune rheumatologic disease, as well as 56 patients with non-autoimmune conditions who were visited in one of the private rheumatology clinics in Saskatoon from January 2010 to the end of December 2010. Information on age, sex, BMI, plasma 25(OH)D, vitamin D and calcium supplement use, serum calcium, serum phosphate, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), glomerular filtration rate (GFR) and season were collected and recorded. We also collected data on disease activity score (DAS 28-ESR) only in cases with rheumatoid arthritis. DAS28-ESR is a quantitative measure of disease activity in rheumatoid arthritis, calculated by using a formula that considers the number of tender joints and swollen joints within 28 joints, as well as ESR [11]. The disease activity is considered high with the score of >5.1, low with